Understanding the Interactions between <i>Staphylococcus aureus</i> and the Raw-Meat-Processing Environment Isolate <i>Klebsiella oxytoca</i> in Dual-Species Biofilms via Discovering an Altered Metabolic Profile
In a raw-meat-processing environment, members of the Enterobacteriaceae family can coexist with <i>Staphylococcus aureus</i> to form dual-species biofilms, leading to a higher risk of food contamination. However, very little is known about the effect of inter-species interactions on dual...
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| Format: | Article |
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MDPI AG
2021-03-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/9/4/672 |
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| author | Xiaoxue Chen Yunan Hu Simin Tian Beizhong Han |
| author_facet | Xiaoxue Chen Yunan Hu Simin Tian Beizhong Han |
| author_sort | Xiaoxue Chen |
| collection | DOAJ |
| description | In a raw-meat-processing environment, members of the Enterobacteriaceae family can coexist with <i>Staphylococcus aureus</i> to form dual-species biofilms, leading to a higher risk of food contamination. However, very little is known about the effect of inter-species interactions on dual-species biofilm formation. The aim of this study was to investigate the interactions between <i>S. aureus</i> and raw-meat-processing environment isolates of <i>Klebsiella oxytoca</i> in dual-species biofilms, by employing an untargeted metabolomics tool. Crystal violet staining assay showed that the biomass of the dual-species biofilm significantly increased and reached its maximum after incubation for 21 h, compared with that of single species grown alone. The number of <i>K. oxytoca</i> in the dual-species biofilm was significantly higher than that of <i>S. aureus</i>. Field emission scanning electron microscopy (FESEM) revealed that both species were evenly distributed, and were tightly wrapped by extracellular polymeric substances in the dual-species biofilms. Ultra-high-pressure liquid chromatography equipped with a quadrupole-time-of-flight mass spectrometer (UHPLC-Q-TOF MS) analysis exhibited a total of 8184 positive ions, and 6294 negative ions were obtained from all test samples. Multivariate data analysis further described altered metabolic profiling between mono- and dual-species biofilms. Further, 18 and 21 different metabolites in the dual-species biofilm were screened as biomarkers by comparing the mono-species biofilms of <i>S. aureus</i> and <i>K. oxytoca</i>, respectively. The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways that were exclusively upregulated in the dual-species biofilm included ABC transporters, amino acid metabolism, and the two-component signal transduction system. Our results contribute to a better understanding of the interactive behavior of inter-species biofilm communities, by discovering altered metabolic profiling. |
| first_indexed | 2024-03-10T12:56:08Z |
| format | Article |
| id | doaj.art-718dc38bb46a43af87bb913990accdb4 |
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| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T12:56:08Z |
| publishDate | 2021-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-718dc38bb46a43af87bb913990accdb42023-11-21T11:52:42ZengMDPI AGMicroorganisms2076-26072021-03-019467210.3390/microorganisms9040672Understanding the Interactions between <i>Staphylococcus aureus</i> and the Raw-Meat-Processing Environment Isolate <i>Klebsiella oxytoca</i> in Dual-Species Biofilms via Discovering an Altered Metabolic ProfileXiaoxue Chen0Yunan Hu1Simin Tian2Beizhong Han3Beijing Laboratory for Food Quality and Safety, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, ChinaBeijing Laboratory for Food Quality and Safety, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, ChinaBeijing Laboratory for Food Quality and Safety, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, ChinaBeijing Laboratory for Food Quality and Safety, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, ChinaIn a raw-meat-processing environment, members of the Enterobacteriaceae family can coexist with <i>Staphylococcus aureus</i> to form dual-species biofilms, leading to a higher risk of food contamination. However, very little is known about the effect of inter-species interactions on dual-species biofilm formation. The aim of this study was to investigate the interactions between <i>S. aureus</i> and raw-meat-processing environment isolates of <i>Klebsiella oxytoca</i> in dual-species biofilms, by employing an untargeted metabolomics tool. Crystal violet staining assay showed that the biomass of the dual-species biofilm significantly increased and reached its maximum after incubation for 21 h, compared with that of single species grown alone. The number of <i>K. oxytoca</i> in the dual-species biofilm was significantly higher than that of <i>S. aureus</i>. Field emission scanning electron microscopy (FESEM) revealed that both species were evenly distributed, and were tightly wrapped by extracellular polymeric substances in the dual-species biofilms. Ultra-high-pressure liquid chromatography equipped with a quadrupole-time-of-flight mass spectrometer (UHPLC-Q-TOF MS) analysis exhibited a total of 8184 positive ions, and 6294 negative ions were obtained from all test samples. Multivariate data analysis further described altered metabolic profiling between mono- and dual-species biofilms. Further, 18 and 21 different metabolites in the dual-species biofilm were screened as biomarkers by comparing the mono-species biofilms of <i>S. aureus</i> and <i>K. oxytoca</i>, respectively. The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways that were exclusively upregulated in the dual-species biofilm included ABC transporters, amino acid metabolism, and the two-component signal transduction system. Our results contribute to a better understanding of the interactive behavior of inter-species biofilm communities, by discovering altered metabolic profiling.https://www.mdpi.com/2076-2607/9/4/672dual-species biofilms<i>Klebsiella oxytoca</i><i>Staphylococcus aureus</i>interactionsmetabolomics |
| spellingShingle | Xiaoxue Chen Yunan Hu Simin Tian Beizhong Han Understanding the Interactions between <i>Staphylococcus aureus</i> and the Raw-Meat-Processing Environment Isolate <i>Klebsiella oxytoca</i> in Dual-Species Biofilms via Discovering an Altered Metabolic Profile Microorganisms dual-species biofilms <i>Klebsiella oxytoca</i> <i>Staphylococcus aureus</i> interactions metabolomics |
| title | Understanding the Interactions between <i>Staphylococcus aureus</i> and the Raw-Meat-Processing Environment Isolate <i>Klebsiella oxytoca</i> in Dual-Species Biofilms via Discovering an Altered Metabolic Profile |
| title_full | Understanding the Interactions between <i>Staphylococcus aureus</i> and the Raw-Meat-Processing Environment Isolate <i>Klebsiella oxytoca</i> in Dual-Species Biofilms via Discovering an Altered Metabolic Profile |
| title_fullStr | Understanding the Interactions between <i>Staphylococcus aureus</i> and the Raw-Meat-Processing Environment Isolate <i>Klebsiella oxytoca</i> in Dual-Species Biofilms via Discovering an Altered Metabolic Profile |
| title_full_unstemmed | Understanding the Interactions between <i>Staphylococcus aureus</i> and the Raw-Meat-Processing Environment Isolate <i>Klebsiella oxytoca</i> in Dual-Species Biofilms via Discovering an Altered Metabolic Profile |
| title_short | Understanding the Interactions between <i>Staphylococcus aureus</i> and the Raw-Meat-Processing Environment Isolate <i>Klebsiella oxytoca</i> in Dual-Species Biofilms via Discovering an Altered Metabolic Profile |
| title_sort | understanding the interactions between i staphylococcus aureus i and the raw meat processing environment isolate i klebsiella oxytoca i in dual species biofilms via discovering an altered metabolic profile |
| topic | dual-species biofilms <i>Klebsiella oxytoca</i> <i>Staphylococcus aureus</i> interactions metabolomics |
| url | https://www.mdpi.com/2076-2607/9/4/672 |
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